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Feedback inhibition controls spike transfer in hybrid thalamic circuits

Nature volume 417, pages 854–858 (2002)Cite this article

Abstract

Sensory information reaches the cerebral cortex through the thalamus, which differentially relays this input depending on the state of arousal1,2,3,4,5. Such ‘gating’ involves inhibition of the thalamocortical relay neurons by the reticular nucleus of the thalamus6,7,8, but the underlying mechanisms are poorly understood. We reconstructed the thalamocortical circuit as an artificial and biological hybrid network in vitro. With visual input simulated as retinal cell activity, we show here that when the gain in the thalamic inhibitory feedback loop is greater than a critical value, the circuit tends towards oscillations—and thus imposes a temporal decorrelation of retinal cell input and thalamic relay output. This results in the functional disconnection of the cortex from the sensory drive, a feature typical of sleep states. Conversely, low gain in the feedback inhibition and the action of noradrenaline, a known modulator of arousal4,9,10, converge to increase input–output correlation in relay neurons. Combining gain control of feedback inhibition and modulation of membrane excitability thus enables thalamic circuits to finely tune the gating of spike transmission from sensory organs to the cortex.

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Figure 1: Design of hybrid thalamic circuits.
Figure 2: Spontaneous spindle activity in ‘sleeping’ hybrid retinothalamic circuit.
Figure 3: The strength of inhibition regulates temporal correlation between input retinal and output TC cell spikes.
Figure 4: Noradrenaline (NA) enhances input–output correlation in TC neurons.

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Acknowledgements

We are grateful to K. Grant, Y. Fregnac, S. Oliet, F. Nagy, A. Destexhe, M. Rudolph and B. Gutkin for in-depth discussion and comments on the manuscript; G. Sadoc, N. Gazère and E. Barbe for their technical input; and A. Destexhe for theoretical simulations. This research was supported by the Groupement d'Intérêt Scientifique Sciences de la Cognition, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Médicale, Plan Pluriformation du Ministère de la Recherche, Fondation pour la Recherche sur l'Epilepsie, and the Institut Electricité Santé de France.

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Authors and Affiliations

  1. Laboratoire de Physiopathologie des Réseaux Neuronaux Médullaires, EPI INSERM 9914, Institut François Magendie, Université Victor Segalen Bordeaux 2, 1 Rue Camille Saint Saëns, 33077, Cedex, Bordeaux, France

    Gwendal Le Masson

  2. Laboratoire IXL, CNRS UMR 5818, ENSEIRB, Université de Bordeaux 1, 351 Cours de la Libération, 33405, Talence Cedex, France

    Sylvie Renaud-Le Masson

  3. Unité de Neurosciences Intégratives et Computationnelles, CNRS UPR 2191, Institut de Neurobiologie Alfred Fessard, 1 Avenue de la Terrasse, 91198, Gif-sur-Yvette Cedex, France

    Damien Debay & Thierry Bal

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Correspondence to Thierry Bal.

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Le Masson, G., Renaud-Le Masson, S., Debay, D. et al. Feedback inhibition controls spike transfer in hybrid thalamic circuits. Nature 417, 854–858 (2002). https://doi.org/10.1038/nature00825

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